Effects of ablation of flocculus and paraflocculus on eye movements in primate

D. S. Zee, A. Yamazaki, P. H. Butler, G. Gucer

Research output: Contribution to journalArticlepeer-review

Abstract

Eye movements were recorded in four rhesus monkeys, before and after bilateral ablations of the flocculi and portions of the paraflocculi ('flocculectomy'). Animals were trained to fixate and follow targets so that pursuit, saccades, and vestibular and optokinetic nystagmus could be quantitated. The vestibuloocular reflex (VOR) was mildly affected by flocculectomy. In darkness the VOR gain (eye velocity/head velocity) for steps of head velocity (normal range, 0.84-0.96) increased postoperatively in one monkey to 1.17, decreased in another to 0.62, and did not change significantly in the other two (0.96, 0.94). VOR phase lead at 0.05-Hz oscillation in darkness (normal range, 0.0-5.0°) increased in two monkeys by 12 and 9.5° but did not change significantly in the others. Visual suppression of inappropriate vestibular nystagmus was impaired. During oscillation at 0.25 Hz with a head-fixed visual scene, the average amount of attenuation of the VOR decreased from 51% preoperatively to 20% postoperatively. Visual suppression of caloric nystagmus was comparably affected. Smooth tracking of small targets moving in space was impaired either with the head still (smooth pursuit) or moving (cancellation of the VOR by fixating a target rotating with the head). The average gain (gaze velocity) in either case was about 0.65 (normal, 0.95-0.98). The pursuit deficit was less than that reported after total cerebellectomy, suggesting other cerebellar structures also participate in smooth tracking. Optokinetic nystagmus (OKN) was present postoperatively but, in response to a constant-velocity stimulus, the initial slowphase velocity decreased by 50% and the rise time to a steady state nearly doubled. For stimuli below 60°/s the average steady-state gain was only mildly diminished to 0.86 (normal 0.98) and the time course of optokinetic afternystagmus (OKAN) in darkness was normal. The response to higher velocity optokinetic stimuli was impaired. These abnormalities can largely be attributed to the coexisting pursuit deficit although the protracted rise to a steady state suggests a change in the ability of the brain stem optokinetic system to handle large amounts of retinal slip. Flocculectomized monkeys showed horizontally, gaze-paretic nystagmus with exponentially decaying centripetal drift (time constant, 1.56 s) and vertically, downbeat nystagmus with exponentially decaying (in three monkeys) or exponentially increasing (in one monkey) slow phases. All animals showed rebound nystagmus. These results implicate the flocculus and possibly the paraflocculus in the control of the time constant and stability of the brain stem oculomotor integrators. Saccadic velocities and accuracy were normal but flocculectomized monkeys showed brief (40-150 ms duration), approximately exponential, postsaccadic drift with amplitudes up to 15% of the size of the saccade. The eyes usually drifted in the same direction as the saccade but each monkey showed an idiosyncratic pattern depending on saccade direction and eye position. Postsaccadic drift may reflect a mismatch between the phasic (pulse) and tonic (step) innervational changes that create saccades. Our results indicate that the flocculus and possibly paraflocculus participate in the control of oculomotor reflexes that insure best visual acuity by preventing retinal slip. The flocculus serves both the specific needs of the fovea (pursuit, saccades, and gaze holding) as well as the phylogenetically older requisite for stabilization of images on the retina during head rotation (VOR and OKN). The unpredictable effect of flocculectomy on VOR gain, postsaccadic drift, and the waveforms of vertical nystagmus may reflect the basic regulatory role of the cerebellum so that inherent imperfections in oculomotor performance are exposed by removal of the flocculus.

Original languageEnglish (US)
Pages (from-to)878-899
Number of pages22
JournalJournal of neurophysiology
Volume46
Issue number4
DOIs
StatePublished - 1981

ASJC Scopus subject areas

  • Neuroscience(all)
  • Physiology

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